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Translational Regulation During Oogenesis and Early Development: the Cap-Poly(A) Tail Relationship

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Translational Regulation During Oogenesis and Early Development: the Cap-Poly(A) Tail Relationship C. R. Biologies 328 (2005) 863–881 http://france.elsevier.com/direct/CRASS3/ Review / Revue Translational regulation during oogenesis and early development: The cap-poly(A) tail relationship Federica Piccioni a, Vincenzo Zappavigna b, Arturo C. Verrotti a,c,∗ a CEINGE–Biotecnologie Avanzate, Via Comunale Margherita 482, 80145 Napoli, Italy b Dipartimento di Biologia Animale, Università di Modena e Reggio Emilia, Via G. Campi 213d, 41100 Modena, Italy c Dipartimento di Biochimica e Biotecnologie Mediche, Università di Napoli “Federico II”, Via S. Pansini 5, 80131 Napoli, Italy Received 27 February 2005; accepted after revision 10 May 2005 Available online 8 June 2005 Presented by Stuart Edelstein Abstract Metazoans rely on the regulated translation of select maternal mRNAs to control oocyte maturation and the initial stages of embryogenesis. These transcripts usually remain silent until their translation is temporally and spatially required during early development. Different translational regulatory mechanisms, varying from cytoplasmic polyadenylation to localization of maternal mRNAs, have evolved to assure coordinated initiation of development. A common feature of these mechanisms is that they share a few key trans-acting factors. Increasing evidence suggest that ubiquitous conserved mRNA-binding factors, including the eukaryotic translation initiation factor 4E (eIF4E) and the cytoplasmic polyadenylation element binding protein (CPEB), interact with cell-specific molecules to accomplish the correct level of translational activity necessary for normal development. Here we review how capping and polyadenylation of mRNAs modulate interaction with multiple regulatory factors, thus controlling translation during oogenesis and early development. To cite this article: F. Piccioni et al., C. R. Biologies 328 (2005). 2005 Académie des sciences. Published by Elsevier SAS. All rights reserved. Keywords: Capping; Polyadenylation; eIF4E; CPEB; Oocyte maturation; Translational regulatory mechanisms; Translational initiation 1. Introduction mal embryogenesis, and germ-line development [1–5]. Translational regulation of an eukaryotic mRNA is Translational control is critical for the proper regu- achieved through the orchestrated action of cis-acting lation of cell cycle, tissue induction and growth, nor- elements and trans-acting factors. Cap-dependent translation in eukaryotes requires the ordered assem- bly of a complex of evolutionarily conserved proteins, * Corresponding author. which starts with the binding of the translation ini- E-mail address: [email protected] (A.C. Verrotti). tiation factor 4E (eIF4E) to the 7-methyl-guanosine 1631-0691/$ – see front matter 2005 Académie des sciences. Published by Elsevier SAS. All rights reserved. doi:10.1016/j.crvi.2005.05.006 864 F. Piccioni et al. / C. R. Biologies 328 (2005) 863–881 (m7GpppN) cap structure at the 5 of the mRNA. Next, complexes involved in translational regulation of spe- the eIF4G factor is recruited allowing additional fac- cific mRNAs have been described and analyzed. tors (PABP, eIF4A, eIF4B, eIF1, eIF1A, eIF2, eIF3, In this review, we will focus on the molecules that among others, and the ribosomal subunits) [6] to form by binding and/or modulating the modifications occur- a complex that, after mRNA circularization, initiates ring at the end of mRNAs, the cap structure at the 5 translation [7–10]. The circularization might become and the poly(A) tail at the 3 end, are the targets of possible once an adequate poly(A) tail is present at the regulatory events that govern translation of select mR- 3-UTR [11]. NAs playing crucial roles in specific developmental eIF4E is the rate-limiting component for cap- processes. dependent translation initiation and therefore repre- sents a major target for translational control [12,13]. eIF4E function can be regulated at different levels by a 2. Structure of eukaryotic mRNAs and variety of molecular processes. First, eIF4E transcrip- translational control tion inside a cell can be increased by growth factor stimuli [14,15]; second, the availability of eIF4E can In the nucleus, eukaryotic mRNAs are first tran- be modulated by the binding to a set of proteins that scribed as precursor mRNAs (pre-mRNAs) and sub- compete with eIF4G, a scaffold protein that aggregates sequently modified by capping, polyadenylation, and the mRNA and the ribosome [16], for eIF4E-binding, splicing. Mature mRNAs are ultimately exported into therefore inhibiting translation initiation [17];third, the cytoplasm where they can be translated into pro- elevated eIF4E activity depends upon its phosphory- teins. Capping of eukaryotic mRNAs involves the addi- lation in response to extracellular stimuli, including tion of a 7-methyl-guanosine residue at the 5 end hormones, growth factors, and mitogens, and corre- to protect this end from nuclease degradation. The lates to an increase in translation rate [16,18].The cap structure in eukaryotes can be of three types function of phosphorylated eIF4E was indeed shown m7GpppNp, m7GpppNmp, m7GpppNmpNmp (m indi- to be necessary for proper growth and development of cates a methyl group attached to the respective nu- Drosophila [19]. cleotide), and is used as a docking point for the cap- During oogenesis in many species, cytoplasmic binding protein complex that mediates the recruitment polyadenylation of a set of maternal mRNAs regu- of the small ribosomal subunit to the 5 end of the lates their translation. A general scheme implies that mRNA. elongation of a short poly(A) tail at the 3 -UTR dur- Polyadenylation occurs after cleavage of the pre- ing development is able to stimulate translation. The mRNA at the 3 end and consists of the addition of up cytoplasmic polyadenylation element binding protein to 250 adenosine residues by the poly(A) polymerase (CPEB) is a sequence-specific RNA interacting factor (PAP) enzyme. Finally, the mechanism of splicing re- that is necessary to achieve adequate poly(A) addition moves all intervening sequences from the pre-mRNA, within the cytoplasm. The rationale for the existence thus producing a mature mRNA that is competent to of a long poly(A) tail is, probably, to allow an mRNA be transported to the cytoplasm. to acquire a circular structure prior to translation ini- Once within the cytoplasm, only mRNAs that are tiation. Increasing evidence indeed suggest that the properly capped and polyadenylated are efficiently structure of an mRNA is essential for proper activity, translated. This has been demonstrated during ooge- including translation efficiency. nesis and early embryogenesis, where regulated cy- The past few years have witnessed considerable toplasmic polyadenylation of mRNAs modulate their advancements in the field of translational control dur- translation. During translation initiation, the cap struc- ing development. In particular, recent studies have re- ture is directly bound by eIF4E, and the poly(A) tail vealed the existence of various translational regula- by the poly(A) binding protein (PABP) in a manner tory mechanisms and identified in the cap-poly(A) tail that induces a synergistic enhancement of translation. interaction the primary target for multiple regulatory Translation that is both cap- and poly(A)-dependent factors. Moreover, novel repressive and stimulatory requires moreover the activity of the eukaryotic ini- F. Piccioni et al. / C. R. Biologies 328 (2005) 863–881 865 tiation translation factor 4G (eIF4G). eIF4G contains nents, the cap-binding protein eIF4E, the adaptor pro- specific binding sites for both eIF4E and PABP, thus tein eIF4G, and the poly(A)-binding protein (PABP). forming a complex that circularizes the mRNA [10]. The direct interaction of eIF4E, bound to eIF4G, to Indeed, mutations that compromise the binding of the cap structure is essential for translation initia- eIF4G with either PABP [20,21] or eIF4E [22,23] af- tion both in vivo and in vitro, while contacts between fect in vitro the synergistic stimulation of translation eIF4G and the poly(A)-bound PABP enhance transla- by the cap structure and the poly(A) tail. In this con- tion (Fig. 1A), but are not strictly required for ribo- text, the 5 cap and the 3 poly(A) tail are modifications some recruitment (see reviews [25–27]). Thus, events necessary for efficient translation. favouring the dissociation of the eIF4E–eIF4G inter- Regulatory sequences and structures within the action significantly impair cap-dependent translation mRNA modulate translation. In addition to the 5 cap and are therefore a potential means for translational and 3 poly(A) tail these include: internal ribosome control. Such a control has indeed been observed entry sites (IRESs), which direct cap-independent both in developmental processes and in tumorigene- translation initiation; upstream open reading frames sis [28,29]. (uORFs), which act as negative regulators by dimin- The functions of eIF4E and the regulation of these ishing translation from the main ORF; secondary depend on the presence on this factor of binding sur- or tertiary structures, like hairpins and pseudoknots, faces for the cap-structure of mRNAs and for vari- which often act by blocking translation initiation; and ous proteins that can modulate its activity. The three- specific binding sequences for multiple regulatory fac- dimensional structure of the eIF4E-cap complex has tors [6]. Many mRNAs are translationally controlled been solved, identifying the relevant molecular con- by sequences in their 5 and 3 untranslated regions tacts between the 5 end of
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